Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways
Seed longevity, the maintenance of viability during storage, is a crucial factor for preservation of genetic resources and ensuring proper seedling establishment and high crop yield. We used a systems biology approach to identify key genes regulating the acquisition of longevity during seed maturati...
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| Veröffentlicht in: | The Plant cell 2015-10, Vol.27 (10), p.2692-2708 |
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| creator | Righetti, Karima Vu, Joseph Ly Pelletier, Sandra Vu, Benoit Ly Glaab, Enrico Lalanne, David Pasha, Asher Patel, Rohan V. Provart, Nicholas J. Verdier, Jerome Leprince, Olivier Buitink, Julia |
| description | Seed longevity, the maintenance of viability during storage, is a crucial factor for preservation of genetic resources and ensuring proper seedling establishment and high crop yield. We used a systems biology approach to identify key genes regulating the acquisition of longevity during seed maturation of Medicago truncatula. Using 104 transcriptomes from seed developmental time courses obtained in five growth environments, we generated a robust, stable coexpression network (MatNet), thereby capturing the conserved backbone of maturation. Using a trait-based gene significance measure, a coexpression module related to the acquisition of longevity was inferred from MatNet. Comparative analysis of the maturation processes in M. truncatula and Arabidopsis thaliana seeds and mining Arabidopsis interaction databases revealed conserved connectivity for 87% of longevity module nodes between both species. Arabidopsis mutant screening for longevity and maturation phenotypes demonstrated high predictive power of the longevity cross-species network. Overrepresentation analysis of the network nodes indicated biological functions related to defense, light, and auxin. Characterization of defense-related wrky3 and nf-x1-like1 (nfxl1) transcription factor mutants demonstrated that these genes regulate some of the network nodes and exhibit impaired acquisition of longevity during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating the activation of defense against pathogens. |
| doi_str_mv | 10.1105/tpc.15.00632 |
| format | Article |
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We used a systems biology approach to identify key genes regulating the acquisition of longevity during seed maturation of Medicago truncatula. Using 104 transcriptomes from seed developmental time courses obtained in five growth environments, we generated a robust, stable coexpression network (MatNet), thereby capturing the conserved backbone of maturation. Using a trait-based gene significance measure, a coexpression module related to the acquisition of longevity was inferred from MatNet. Comparative analysis of the maturation processes in M. truncatula and Arabidopsis thaliana seeds and mining Arabidopsis interaction databases revealed conserved connectivity for 87% of longevity module nodes between both species. Arabidopsis mutant screening for longevity and maturation phenotypes demonstrated high predictive power of the longevity cross-species network. Overrepresentation analysis of the network nodes indicated biological functions related to defense, light, and auxin. Characterization of defense-related wrky3 and nf-x1-like1 (nfxl1) transcription factor mutants demonstrated that these genes regulate some of the network nodes and exhibit impaired acquisition of longevity during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating the activation of defense against pathogens.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.15.00632</identifier><identifier>PMID: 26410298</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - physiology ; Arabidopsis thaliana ; Biological Evolution ; Datasets ; Developmental biology ; Environment ; Gene expression regulation ; Gene Expression Regulation, Plant ; Gene Regulatory Networks ; Genes ; Germination ; Large-Scale Biology ; LARGE-SCALE BIOLOGY ARTICLE ; Life Sciences ; Longevity ; Medicago truncatula ; Medicago truncatula - genetics ; Medicago truncatula - growth & development ; Medicago truncatula - physiology ; Mutation ; Pathogens ; Phenotype ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants ; Seed longevity ; Seeds ; Seeds - genetics ; Seeds - growth & development ; Seeds - physiology ; Time Factors ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcriptome</subject><ispartof>The Plant cell, 2015-10, Vol.27 (10), p.2692-2708</ispartof><rights>2015 American Society of Plant Biologists</rights><rights>2015 American Society of Plant Biologists. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2015 American Society of Plant Biologists. All rights reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c485t-996f15888cabb33753c5a51432cb9814fe24db73b1fac35a4f1a385eb53568623</citedby><orcidid>0000-0002-1457-764X ; 0000-0003-3977-7469 ; 0000-0001-7582-2939 ; 0009-0004-6166-270X ; 0000-0003-3039-2159 ; 0000-0003-1414-8690</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/plantcell.27.10.2692$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/plantcell.27.10.2692$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,781,785,804,886,27928,27929,58021,58254</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26410298$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01392707$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Righetti, Karima</creatorcontrib><creatorcontrib>Vu, Joseph Ly</creatorcontrib><creatorcontrib>Pelletier, Sandra</creatorcontrib><creatorcontrib>Vu, Benoit Ly</creatorcontrib><creatorcontrib>Glaab, Enrico</creatorcontrib><creatorcontrib>Lalanne, David</creatorcontrib><creatorcontrib>Pasha, Asher</creatorcontrib><creatorcontrib>Patel, Rohan V.</creatorcontrib><creatorcontrib>Provart, Nicholas J.</creatorcontrib><creatorcontrib>Verdier, Jerome</creatorcontrib><creatorcontrib>Leprince, Olivier</creatorcontrib><creatorcontrib>Buitink, Julia</creatorcontrib><title>Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Seed longevity, the maintenance of viability during storage, is a crucial factor for preservation of genetic resources and ensuring proper seedling establishment and high crop yield. We used a systems biology approach to identify key genes regulating the acquisition of longevity during seed maturation of Medicago truncatula. Using 104 transcriptomes from seed developmental time courses obtained in five growth environments, we generated a robust, stable coexpression network (MatNet), thereby capturing the conserved backbone of maturation. Using a trait-based gene significance measure, a coexpression module related to the acquisition of longevity was inferred from MatNet. Comparative analysis of the maturation processes in M. truncatula and Arabidopsis thaliana seeds and mining Arabidopsis interaction databases revealed conserved connectivity for 87% of longevity module nodes between both species. Arabidopsis mutant screening for longevity and maturation phenotypes demonstrated high predictive power of the longevity cross-species network. Overrepresentation analysis of the network nodes indicated biological functions related to defense, light, and auxin. Characterization of defense-related wrky3 and nf-x1-like1 (nfxl1) transcription factor mutants demonstrated that these genes regulate some of the network nodes and exhibit impaired acquisition of longevity during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating the activation of defense against pathogens.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis thaliana</subject><subject>Biological Evolution</subject><subject>Datasets</subject><subject>Developmental biology</subject><subject>Environment</subject><subject>Gene expression regulation</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Germination</subject><subject>Large-Scale Biology</subject><subject>LARGE-SCALE BIOLOGY ARTICLE</subject><subject>Life Sciences</subject><subject>Longevity</subject><subject>Medicago truncatula</subject><subject>Medicago truncatula - genetics</subject><subject>Medicago truncatula - growth & development</subject><subject>Medicago truncatula - physiology</subject><subject>Mutation</subject><subject>Pathogens</subject><subject>Phenotype</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Seed longevity</subject><subject>Seeds</subject><subject>Seeds - genetics</subject><subject>Seeds - growth & development</subject><subject>Seeds - physiology</subject><subject>Time Factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcriptome</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkktvEzEUhUcIREthxxp5CRIT_BjPeDZIJUAbKTyUgsTO8jjXqduJHWxPSv4TPxIPKeGxYWXL97vn3iOfonhM8IQQzF-kjZ4QPsG4ZvROcUw4oyVtxZe7-Y4rXFY1J0fFgxivMMakIe394ojWFcEZOi6-z5yBAE4D8gbNvVvB1qZduYBeJViiM3AQkQl-jRRa-G6ICU09fNsEiNF6h95DuvHheuy-gNzwTqUhqDSWZktwyRqbBRawGrKgDxHNrbu2brWnL_KT6myfR6Lk0Svrk9XoNRhwEQ5LfFTp8kbt4sPinlF9hEe350nx-e2bT9Pzcv7hbDY9nZe6EjyVbVsbwoUQWnUdYw1nmitOKkZ11wpSGaDVsmtYR4zSjKvKEMUEh44zXouaspPi5V53M3RrWOpsI6heboJdq7CTXln5d8XZS7nyW1nVgjKGs8CzvcDlP23np3M5vmHCWtrgZksy-_R2WPBfB4hJrm3U0PfKgR-iJAKLummJEP9HG0Ya0dbVaOH5HtXBxxjAHNYgWI65kTk3knD5MzcZf_Kn4wP8Kyi_HV3F_GWH-iaPTuMGkjajMq1byn4A2NnP0w</recordid><startdate>20151001</startdate><enddate>20151001</enddate><creator>Righetti, Karima</creator><creator>Vu, Joseph Ly</creator><creator>Pelletier, Sandra</creator><creator>Vu, Benoit Ly</creator><creator>Glaab, Enrico</creator><creator>Lalanne, David</creator><creator>Pasha, Asher</creator><creator>Patel, Rohan V.</creator><creator>Provart, Nicholas J.</creator><creator>Verdier, Jerome</creator><creator>Leprince, Olivier</creator><creator>Buitink, Julia</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Biologists (ASPB)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1457-764X</orcidid><orcidid>https://orcid.org/0000-0003-3977-7469</orcidid><orcidid>https://orcid.org/0000-0001-7582-2939</orcidid><orcidid>https://orcid.org/0009-0004-6166-270X</orcidid><orcidid>https://orcid.org/0000-0003-3039-2159</orcidid><orcidid>https://orcid.org/0000-0003-1414-8690</orcidid></search><sort><creationdate>20151001</creationdate><title>Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways</title><author>Righetti, Karima ; 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Characterization of defense-related wrky3 and nf-x1-like1 (nfxl1) transcription factor mutants demonstrated that these genes regulate some of the network nodes and exhibit impaired acquisition of longevity during maturation. These data suggest that seed longevity evolved by co-opting existing genetic pathways regulating the activation of defense against pathogens.</abstract><cop>England</cop><pub>American Society of Plant Biologists</pub><pmid>26410298</pmid><doi>10.1105/tpc.15.00632</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-1457-764X</orcidid><orcidid>https://orcid.org/0000-0003-3977-7469</orcidid><orcidid>https://orcid.org/0000-0001-7582-2939</orcidid><orcidid>https://orcid.org/0009-0004-6166-270X</orcidid><orcidid>https://orcid.org/0000-0003-3039-2159</orcidid><orcidid>https://orcid.org/0000-0003-1414-8690</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - physiology Arabidopsis thaliana Biological Evolution Datasets Developmental biology Environment Gene expression regulation Gene Expression Regulation, Plant Gene Regulatory Networks Genes Germination Large-Scale Biology LARGE-SCALE BIOLOGY ARTICLE Life Sciences Longevity Medicago truncatula Medicago truncatula - genetics Medicago truncatula - growth & development Medicago truncatula - physiology Mutation Pathogens Phenotype Plant Proteins - genetics Plant Proteins - metabolism Plants Seed longevity Seeds Seeds - genetics Seeds - growth & development Seeds - physiology Time Factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptome |
| title | Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways |
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